Links between the detritivore and the herbivore system: effects of earthworms and Collembola on plant growth and aphid development

Abstract

Effects of Collembola (Heteromurus nitidus and Onychiurus scotarius) and earthworms (Aporrectodea caliginosa and Octolasion tyrtaeum) on the growth of two plant species from different functional groups (Poa annua and Trifolium repens), and on the development of aphids (Myzus persicae) were investigated in a laboratory experiment lasting 20 weeks. Using soil from a fallow site which had been set aside for about 15 years, we expected that nitrogen would be of limited supply to plants and hypothesized that the soil animals studied, particularly earthworms, would increase nutrient availability to plants and thereby also modify aphid reproduction and development. Plant growth was modified strongly by the presence of soil animals. Earthworms caused a more than twofold increase in shoot and root mass of P. annua but increased that of T. repens by only 18% and 6%, respectively. However, earthworms neither affected plant shoot/root ratio nor the nitrogen concentration in plant tissue. In contrast, the presence of Collembola caused a reduction in plant biomass particularly that of P. annua roots, but plant tissue nitrogen concentration was increased, although only slightly. Aphid reproduction on T. repens was lowered in the presence of Collembola on average by 45% but on P. annua increased by a factor of about 3. It is concluded that Collembola decrease aphid reproduction on more palatable host plants like T. repens but increase that on less palatable ones like P. annua. Earthworm presence also affected aphid reproduction but the effect was less consistent than that of Collembola. In the presence of earthworms, aphid reproduction was in one experimental period increased by some 70%. Earthworms also modified the numbers of Collembola and their vertical distribution in experimental chambers. Exploitation of deeper soil layers by H. nitidus was increased but, generally, O. scotarius numbers were reduced whereas those of H. nitidus increased in earthworm treatments. The presence of Collembola also influenced earthworm body mass during the experiment. In general it declined, but in the presence of Collembola loss of body mass of A. caliginosa was more pronounced. We conclude that inhibiting effects between Collembola and earthworms resulted from the use of a common resource, litter material rich in nitrogen. This is supported by the higher C/N ratio of the litter material in the presence of earthworms and Collembola by the end of the experiment. Effects of soil invertebrates like Collembola and earthworms on plant performance and aphid development are assumed to be modified by complex direct and indirect interactions among soil animal groups.